Host specificity in South African mistletoes.
Okubamichael, Desale Yosief.
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Mistletoes intimately connect to their host trees with a haustorium that allows them to access nutrients and water. Mistletoes in South Africa vary greatly in their degree of host specificity. Most species occur on a wide range of host families, while others are restricted to a single host family or—at the extreme—to a single host species. Mistletoes that are host generalists at a larger spatial scale may become host-specific at a local scale. One of the challenges in mistletoe biology is determining the factors that maintain local host specificity. Birds potentially reinforce the mistletoe–host interactions by direct dispersal. However, many mistletoe species coexist while parasitising different co-occurring host species. This suggests that host trees may impose more selection pressure than birds in determining host specificity. Thus, my thesis examines the role of host trees as ecological and physiological filters that influence the infection patterns and determine host specificity of mistletoes in South Africa. The second chapter of this thesis synthesises the literature on host specificity in mistletoes. I then present the results of four field and laboratory experiments that were used examine the features affecting host specificity in representatives of two families of mistletoes (Loranthaceae and Viscaceae) in South Africa. My main research objectives focus on host abundance and morphology, host compatibility, host water and nutrient content, abiotic influences on mistletoe seedling survival and growth and mistletoe–host stomatal morphology in relation to water potential that affect nutrient acquisition by mistletoes from their host trees. The geographic mosaic approach was explored as a potential explanation for the mistletoe–host interactions that direct host specificity in mistletoes. I synthesised the available literature on the mechanisms and factors that direct mistletoe host specificity. This was supported by data analysed from South African herbarium collections, books describing the South African flora and field observations in South Africa. I suggest that host abundance (host availability through time and space) and host compatibility (as determined by genetic, morphological, physiological and chemical factors) play a primary role in determining host specificity in South African mistletoes, while differential bird dispersal strengthens or weakens mistletoe–host interactions. Analysis of the network structure of mistletoe–host interactions at different levels (e.g., at the level of population, species and genus) followed by genetic and reciprocal germination experiments may reveal the patterns and mechanisms of host specificity in mistletoes. I quantified the mistletoe–host composition, height of potential host trees and nutrient and water content of mistletoes and their hosts at Pniel Estates. Surveys of the study site revealed a single mistletoe species, Viscum rotundifolium, parasitising only Ziziphus mucronata and Ehretia rigida. Both parasitised host species were not the most abundant trees, were not the tallest trees and did not have the highest water or nutrient content of trees in the area, although these factors have been found to be good predictors for mistletoe parasitism in other studies. Subsequently, I tested mistletoe–host compatibility by conducting a germination experiment in the greenhouse by inculcating seeds of V. rotundifolium on freshly cut branches of nine available potential host trees. I found that mistletoe seeds had a greater chance of attachment and subsequent survival on branches of E. rigida and Z. mucronata as compared with seeds on co-occurring Acacia and other potential host species. This suggests that host compatibility plays a role in directing the host specificity of V. rotundifolium at Pniel Estates. I found that individuals of V. rotundifolium had more negative water potentials than their host trees and, by doing so, they passively maintain the flow of nutrients. In addition, I found evidence that the mistletoe uses active uptake to access nutrients from host phloem because the leaf tissue of a mistletoe had a nitrogen-to-calcium ratio (N:Ca) >1. Conventionally, a high N:Ca ratio (>1) in the leaf tissue of a mistletoe is taken as evidence of active uptake from host phloem because N is highly phloem-mobile while Ca is a large molecule and is phloem-immobile. This method has shortcomings discussed at greater length in the chapter but my findings suggest that the mistletoe V. rotundifolium uses a combination of passive and active nutrient uptake. I quantified the mistletoe–host community composition and host physical features (height and diameter at breast height) in two sites in KwaZulu-Natal, South Africa—Highover and Mtontwane. The mistletoe Agelanthus natalitius (Loranthaceae) is common at both sites, parasitising the most abundant host species—Acacia karroo—and the second most abundant host tree—Acacia caffra. Prevalence of mistletoe infection (percentage of trees parasitised) was positively correlated with tree size (height and diameter at breast height). The two host species did not differ significantly in height. At Highover the host species A. caffra and A. karroo had a similar prevalence of mistletoe infection but at Mtontwane a significantly higher percentage of A. caffra trees was parasitised in comparison with A. karroo. However, the intensity of mistletoe infection (mean number of mistletoes per tree) was lower for A. caffra (Highover: 0.66 ± 0.01, Mtontwane: 0.89 ± 0.04) than for A. karroo (Highover: 0.73 ± 0.04, Mtontwane: 1.03 ± 0.64). There were two highly infected big trees in Highover and one in Mtontwane where many mistletoe-dispersing birds were nesting which inflated the numbers for intensity of mistletoe infection in A. caffra, however. I tested mistletoe–host compatibility by conducting a reciprocal transplant experiment in the two study sites. I applied a paired design, using one local and one non-local mistletoe seed in each pair, with seed pairs placed on the two main host species at the different sites. Except in Highover where an unidentified pathogen retarded growth and survival, mistletoe seeds placed on the same substrate and in the same site as their source host grew a longer hypocotyl and had greater survival. Regardless of source, mistletoes placed on A. karroo had longer hypocotyls and greater survival than mistletoes on A. caffra. These results suggest that there may be adaptation of the mistletoe Agelanthus natalitius to the most frequently encountered host species, Acacia karroo. To simulate the conditions encountered by mistletoes during the dry and cold South African winter, mistletoe seedlings were monitored at different levels of microclimate (light, temperature and moisture) in a growth chamber. I found that higher light availability (20% and 40% shade versus 80% shade), cool temperatures (15°C and 20°C versus 25°C) and continuous moisture availability improved seedling development and subsequent survival of two mistletoe species (Viscum rotundifolium and Agelanthus natalitius). I studied the leaf stomata of two host–mistletoe pairs (Acacia karroo–Agelanthus natalitius and Vitex obovata–Erianthemum dregei) using a scanning electron microscope to investigate some of the underlying mechanisms that enable mistletoes to maintain more negative water potentials than their host trees and at the same time control water loss. In addition, I examined the response of mistletoes to the application of abscisic acid (ABA), a plant growth regulator that controls stomatal closure. I found that the mistletoes had a higher density of stomata and had larger stomata than their host trees. In addition, both mistletoe and host leaves closed their stomata during midday and in response to exogenous ABA. The ability of mistletoes to control water loss in this way may be one reason why mistletoes rarely kill their host trees, which would be maladaptive. The mistletoes used in my studies are known to be host generalists at a larger spatial scale but I found that they were host specific at a local scale. The results of my research suggest that host abundance and compatibility play a role in directing host specificity, while host nutrient and water status have little effect on host specificity at this local scale. The interactions between the generalist mistletoes used in my studies and their hosts are likely to vary over the geographic ranges of the mistletoe and alternate among different hosts. This may create multiple locally host–specific mistletoe populations and produce a complex geographic mosaic of mistletoe–host combinations across space and time. I suggest that mistletoe populations in South Africa may comprise numerous lineages incapable of parasitising the full range of host species, which could potentially lead to the formation of distinct host races over time. In the future, it would be interesting to document the infection patterns of these generalist mistletoe species across their entire geographic ranges in southern Africa, with particular focus on the patterns of mistletoe infection in places where the host abundance changes among sites. Host preferences may vary with changes in host frequency and host community composition. This could be paired with reciprocal transplant germination experiments in several sites to ascertain whether the mistletoe species have higher fitness on the most locally abundant hosts.
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